Epigenetic regulation of histone modifications and Gata6 gene expression induced by maternal diet in mouse embryoid bodies in a model of developmental programming

详细信息    查看全文

• 作者：Congshan Sun (1)
  Oleg Denisenko (2)
  Bhavwanti Sheth (1)
  Andy Cox (1)
  Emma S Lucas (1)
  Neil R Smyth (1)
  Tom P Fleming (1)
  
  1. Centre for Biological Sciences ; University of Southampton ; Mailpoint 840 ; Level D Lab & Path Block ; Southampton General Hospital ; Tremona Road ; Southampton ; SO16 6YD ; UK
  2. Department of Medicine ; University of Washington ; Seattle ; WA ; 98109 ; USA
  
• 关键词：Maternal low protein diet ; Embryoid body ; Mouse blastocyst ; Histone epigenetics ; Metabolic disease ; Gata6 ; Primitive endoderm ; Chromatin immunoprecipitation
• 刊名：BMC Developmental Biology
• 出版年：2015
• 出版时间：December 2015
• 年：2015
• 卷：15
• 期：1
• 全文大小：1,062 KB
• 参考文献：1. Fleming TP, Kwong WY, Porter R, Ursell E, Fesenko I, Wilkins A, et al. The embryo and its future. Biol Reprod. 2004;71(4):1046鈥?4. CrossRef
  2. Fleming TP, Velazquez MA, Eckert JJ, Lucas ES, Watkins AJ. Nutrition of females during the peri-conceptional period and effects on foetal programming and health of offspring. Anim Reprod Sci. 2012;130(3鈥?):193鈥?. CrossRef
  3. Steegers-Theunissen RP, Twigt J, Pestinger V, Sinclair KD. The periconceptional period, reproduction and long-term health of offspring: the importance of one-carbon metabolism. Hum Reprod Update. 2013;19(6):640鈥?5. CrossRef
  4. Barker DJ. The origins of the developmental origins theory. J Intern Med. 2007;261(5):412鈥?. 2796.2007.01809.x" target="_blank" title="It opens in new window">CrossRef
  5. Barker DJ, Thornburg KL. The obstetric origins of health for a lifetime. Clin Obstet Gynecol. 2013;56(3):511鈥?. CrossRef
  6. Langley-Evans SC. Fetal programming of CVD and renal disease: animal models and mechanistic considerations. Proc Nutr Soc. 2013;72(3):317鈥?5. CrossRef
  7. Hanson MA, Gluckman PD. Developmental origins of health and disease: new insights. Basic Clin Pharmacol Toxicol. 2008;102(2):90鈥?. CrossRef
  8. Kwong WY, Wild AE, Roberts P, Willis AC, Fleming TP. Maternal undernutrition during the preimplantation period of rat development causes blastocyst abnormalities and programming of postnatal hypertension. Development. 2000;127(19):4195鈥?02.
  9. Watkins AJ, Ursell E, Panton R, Papenbrock T, Hollis L, Cunningham C, et al. Adaptive responses by mouse early embryos to maternal diet protect fetal growth but predispose to adult onset disease. Biol Reprod. 2008;78(2):299鈥?06. CrossRef
  10. Eckert JJ, Porter R, Watkins AJ, Burt E, Brooks S, Leese HJ, et al. Metabolic induction and early responses of mouse blastocyst developmental programming following maternal low protein diet affecting life-long health. PLoS One. 2012;7(12):e52791. 2791" target="_blank" title="It opens in new window">CrossRef
  11. Sun C, Velazquez MA, Marfy-Smith S, Sheth B, Cox A, Johnston DA, et al. Mouse early extra-embryonic lineages activate compensatory endocytosis in response to poor maternal nutrition. Development. 2014;141(5):1140鈥?0. CrossRef
  12. Coan PM, Vaughan OR, McCarthy J, Mactier C, Burton GJ, Constancia M, et al. Dietary composition programmes placental phenotype in mice. J Physiol. 2011;589(Pt 14):3659鈥?0. CrossRef
  13. Young LE, Fernandes K, McEvoy TG, Butterwith SC, Gutierrez CG, Carolan C, et al. Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture. Nat Genet. 2001;27(2):153鈥?. CrossRef
  14. Fernandez-Gonzalez R, Moreira P, Bilbao A, Jimenez A, Perez-Crespo M, Ramirez MA, et al. Long-term effect of in vitro culture of mouse embryos with serum on mRNA expression of imprinting genes, development, and behavior. Proc Natl Acad Sci U S A. 2004;101(16):5880鈥?. CrossRef
  15. Mann MR, Lee SS, Doherty AS, Verona RI, Nolen LD, Schultz RM, et al. Selective loss of imprinting in the placenta following preimplantation development in culture. Development. 2004;131(15):3727鈥?5. CrossRef
  16. Morgan HD, Jin XL, Li A, Whitelaw E, O'Neill C. The culture of zygotes to the blastocyst stage changes the postnatal expression of an epigentically labile allele, agouti viable yellow, in mice. Biol Reprod. 2008;79(4):618鈥?3. CrossRef
  17. Rivera RM, Stein P, Weaver JR, Mager J, Schultz RM, Bartolomei MS. Manipulations of mouse embryos prior to implantation result in aberrant expression of imprinted genes on day 9.5 of development. Hum Mol Genet. 2008;17(1):1鈥?4. CrossRef
  18. Rossant J, Chazaud C, Yamanaka Y. Lineage allocation and asymmetries in the early mouse embryo. Philos Trans R Soc Lond B Biol Sci. 2003;358(1436):1341鈥?. discussion 1349. CrossRef
  19. Schrode N, Saiz N, Di Talia S, Hadjantonakis AK. GATA6 levels modulate primitive endoderm cell fate choice and timing in the mouse blastocyst. Dev Cell. 2014;29(4):454鈥?7. CrossRef
  20. Artus J, Piliszek A, Hadjantonakis AK. The primitive endoderm lineage of the mouse blastocyst: sequential transcription factor activation and regulation of differentiation by Sox17. Dev Biol. 2011;350(2):393鈥?04. CrossRef
  21. Morrisey EE, Musco S, Chen MY, Lu MM, Leiden JM, Parmacek MS. The gene encoding the mitogen-responsive phosphoprotein Dab2 is differentially regulated by GATA-6 and GATA-4 in the visceral endoderm. J Biol Chem. 2000;275(26):19949鈥?4. CrossRef
  22. Sun-Wada GH, Manabe S, Yoshimizu T, Yamaguchi C, Oka T, Wada Y, et al. Upstream regions directing heart-specific expression of the GATA6 gene during mouse early development. J Biochem. 2000;127(4):703鈥?. CrossRef
  23. Caslini C, Capo-chichi CD, Roland IH, Nicolas E, Yeung AT, Xu XX. Histone modifications silence the GATA transcription factor genes in ovarian cancer. Oncogene. 2006;25(39):5446鈥?1. CrossRef
  24. Bartova E, Krejci J, Harnicarova A, Galiova G, Kozubek S. Histone modifications and nuclear architecture: a review. J Histochem Cytochem. 2008;56(8):711鈥?1. CrossRef
  25. Liu X, Zhao D, Zheng Y, Wang L, Qian Y, Xu C, et al. Expression of histone acetyltransferase GCN5 and histone deacetylase 1 in the cultured mouse preimplantation embryos. Curr Pharm Des. 2014;20(11):1772鈥?. CrossRef
  26. Leahy A, Xiong JW, Kuhnert F, Stuhlmann H. Use of developmental marker genes to define temporal and spatial patterns of differentiation during embryoid body formation. J Exp Zool. 1999;284(1):67鈥?1. CrossRef
  27. Doughton G, Wei J, Tapon N, Welham MJ, Chalmers AD. Formation of a polarised primitive endoderm layer in embryoid bodies requires fgfr/erk signalling. PLoS One. 2014;9(4):e95434. CrossRef
  28. Chlon TM, Crispino JD. Combinatorial regulation of tissue specification by GATA and FOG factors. Development. 2012;139(21):3905鈥?6. CrossRef
  29. Molkentin JD. The zinc finger-containing transcription factors GATA-4, 鈭?, and 鈭?. Ubiquitously expressed regulators of tissue-specific gene expression. J Biol Chem. 2000;275(50):38949鈥?2. CrossRef
  30. Capo-chichi CD, Roland IH, Vanderveer L, Bao R, Yamagata T, Hirai H, et al. Anomalous expression of epithelial differentiation-determining GATA factors in ovarian tumorigenesis. Cancer Res. 2003;63(16):4967鈥?7.
  31. Cai KQ, Caslini C, Capo-chichi CD, Slater C, Smith ER, Wu H, et al. Loss of GATA4 and GATA6 expression specifies ovarian cancer histological subtypes and precedes neoplastic transformation of ovarian surface epithelia. PLoS One. 2009;4(7):e6454. CrossRef
  32. Morrisey EE, Tang Z, Sigrist K, Lu MM, Jiang F, Ip HS, et al. GATA6 regulates HNF4 and is required for differentiation of visceral endoderm in the mouse embryo. Genes Dev. 1998;12(22):3579鈥?0. CrossRef
  33. Capo-Chichi CD, Smedberg JL, Rula M, Nicolas E, Yeung AT, Adamo RF, et al. Alteration of Differentiation Potentials by Modulating GATA Transcription Factors in Murine Embryonic Stem Cells. Stem Cells Int. 2010;2010:602068. CrossRef
  34. Padua MB, Fox SC, Jiang T, Morse DA, Tevosian SG. Simultaneous gene deletion of gata4 and gata6 leads to early disruption of follicular development and germ cell loss in the murine ovary. Biol Reprod. 2014;91(1):24. CrossRef
  35. Carrasco M, Delgado I, Soria B, Martin F, Rojas A. GATA4 and GATA6 control mouse pancreas organogenesis. J Clin Invest. 2012;122(10):3504鈥?5. CrossRef
  36. Zhao R, Watt AJ, Battle MA, Li J, Bondow BJ, Duncan SA. Loss of both GATA4 and GATA6 blocks cardiac myocyte differentiation and results in acardia in mice. Dev Biol. 2008;317(2):614鈥?. CrossRef
  37. Yang DH, Cai KQ, Roland IH, Smith ER, Xu XX. Disabled-2 is an epithelial surface positioning gene. J Biol Chem. 2007;282(17):13114鈥?2. CrossRef
  38. Capo-Chichi CD, Rula ME, Smedberg JL, Vanderveer L, Parmacek MS, Morrisey EE, et al. Perception of differentiation cues by GATA factors in primitive endoderm lineage determination of mouse embryonic stem cells. Dev Biol. 2005;286(2):574鈥?6. CrossRef
  39. Watkins AJ, Platt D, Papenbrock T, Wilkins A, Eckert JJ, Kwong WY, et al. Mouse embryo culture induces changes in postnatal phenotype including raised systolic blood pressure. Proc Natl Acad Sci U S A. 2007;104(13):5449鈥?4. CrossRef
  40. Yasuda E, Seki Y, Higuchi T, Nakashima F, Noda T, Kurosawa H. Development of cystic embryoid bodies with visceral yolk-sac-like structures from mouse embryonic stem cells using low-adherence 96-well plate. J Biosci Bioeng. 2009;107(4):442鈥?. CrossRef
  41. Lucas ES, Watkins AJ, Cox AL, Marfy-Smith SJ, Smyth N, Fleming TP. Tissue-specific selection of reference genes is required for expression studies in the mouse model of maternal protein undernutrition. Theriogenology. 2011;76(3):558鈥?9. CrossRef
  42. Flanagin S, Nelson JD, Castner DG, Denisenko O, Bomsztyk K. Microplate-based chromatin immunoprecipitation method, Matrix ChIP: a platform to study signaling of complex genomic events. Nucleic Acids Res. 2008;36(3):e17. CrossRef
  
• 刊物主题：Developmental Biology; Animal Models; Life Sciences, general;
• 出版者：BioMed Central
• ISSN：1471-213X

文摘

Background Dietary interventions during pregnancy alter offspring fitness. We have shown mouse maternal low protein diet fed exclusively for the preimplantation period (Emb-LPD) before return to normal protein diet (NPD) for the rest of gestation, is sufficient to cause adult offspring cardiovascular and metabolic disease. Moreover, Emb-LPD blastocysts sense altered nutrition within the uterus and activate compensatory cellular responses including stimulated endocytosis within extra-embryonic trophectoderm and primitive endoderm (PE) lineages to protect fetal growth rate. However, these responses associate with later disease. Here, we investigate epigenetic mechanisms underlying nutritional programming of PE that may contribute to its altered phenotype, stabilised during subsequent development. We use embryonic stem (ES) cell lines established previously from Emb-LPD and NPD blastocysts that were differentiated into embryoid bodies (EBs) with outer PE-like layer. Results Emb-LPD EBs grow to a larger size than NPD EBs and express reduced Gata6 transcription factor (regulator of PE differentiation) at mRNA and protein levels, similar to Emb-LPD PE derivative visceral yolk sac tissue in vivo in later gestation. We analysed histone modifications at the Gata6 promoter in Emb-LPD EBs using chromatin immunoprecipitation assay. We found significant reduction in histone H3 and H4 acetylation and RNA polymerase II binding compared with NPD EBs, all markers of reduced transcription. Other histone modifications, H3K4Me2, H3K9Me3 and H3K27Me3, were unaltered. A similar but generally non-significant histone modification pattern was found on the Gata4 promoter. Consistent with these changes, histone deacetylase Hdac-1, but not Hdac-3, gene expression was upregulated in Emb-LPD EBs. Conclusions First, these data demonstrate ES cells and EBs retain and propagate nutritional programming adaptations in vitro, suitable for molecular analysis of mechanisms, reducing animal use. Second, they reveal maternal diet induces persistent changes in histone modifications to regulate Gata6 expression and PE growth and differentiation that may affect lifetime health.